Invasion Risks Posed by Ornamental Freshwater Fish Trade to Southeastern Brazilian Rivers
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Neotropical Ichthyology, 11(2):433-441, 2013 Copyright © 2013 Sociedade Brasileira de Ictiologia Invasion risks posed by ornamental freshwater fish trade to southeastern Brazilian rivers André Lincoln Barroso de Magalhães1 and Claudia Maria Jacobi2 A model was developed to assess the risk of invasion of ornamental non-native fishes to six rivers in the state of Minas Gerais, southeastern Brazil, with focus on species popularity. Thirty-nine aquarium shops, in six cities, were visited monthly from January to December 2007. In each city, fish species were identified, and their biology and invasion history information was obtained from the literature. We calculated the annual frequency of occurrence and average number of specimens monthly available in stores. Quarterly water temperature and dissolved oxygen data from 1997 to 2007 were obtained for the Velhas, Muriaé, Uberabinha, Sapucaí-Mirim, Doce and Todos os Santos Rivers from public databases. The invasion risk of each species was assessed through a model comprising nine parameters grouped in four variables: (i) Invasiveness (thermal and dissolved oxygen ranges, diet, parental care or fecundity), (ii) History of invasions (establishment), (iii) Propagule pressure (commercial success, comprising annual frequency of occurrence and number of specimens available monthly at stores), and (iv) Invasibility (water temperature and dissolved oxygen in the target river compatible with the species ranges). Of the 345 ornamental fish species for sale, 332 are non-native to either Minas Gerais (n = 151) or Brazil (n = 194). Based on the proposed cutting values, in particular the compatibility between species and recipient thermal ranges, five ornamental non-native species (Cyprinus rubrofuscus, Carassius auratus, Xiphophorus hellerii, Poecilia reticulata, and P. latipinna) can potentially invade the Velhas and Muriaé Rivers, four species (Cyprinus rubrofuscus, Carassius auratus, X. helleri, and P. reticulata) the Uberabinha River, four species (Cyprinus rubrofuscus, Carassius auratus, X. maculatus, and P. reticulata) the Sapucaí-Mirim River, three species (Carassius auratus, X. hellerii, and P. reticulata) the Doce River, and three species (Cyprinus rubrofuscus, P. reticulata, and Amatitlania nigrofasciata) can potentially invade the Todos os Santos River. Six recommendations are suggested to reduce the invasion risk of non-native fish on the rivers surveyed posed by aquarium trade. Um modelo foi desenvolvido para avaliar o risco de invasão de peixes ornamentais não-nativos em seis rios do estado de Minas Gerais, sudeste do Brasil, com foco na popularidade das espécies. Trinta e nove lojas de aquário em seis cidades foram visitadas mensalmente de janeiro a dezembro de 2007. Em cada cidade, as espécies foram identificadas e suas biologias e histórias de invasão foram obtidas da literatura. Calculou-se a frequência de ocorrência anual e quantidade média mensal de exemplares disponíveis nas lojas. Foram obtidas temperaturas trimestrais da água e dados de oxigênio dissolvido de 1997 a 2007 dos rios Velhas, Muriaé, Uberabinha, Sapucaí-Mirim, Doce e Todos os Santos a partir de bases de dados públicas. O risco de invasão de cada espécie foi avaliado através de um modelo composto por nove parâmetros agrupados em quatro variáveis: (i) Invasividade (limite de alcance térmico/oxigênio dissolvido, dieta, cuidado parental ou fecundidade), (ii) Histórico de invasões (estabelecimento), (iii) Pressão de propágulos (sucesso comercial, composto pela frequência de ocorrência anual e número de exemplares disponíveis mensalmente nas lojas), e (iv) Invasibilidade (temperatura da água/oxigênio dissolvido dos rios compatível com o limite de alcance térmico/ oxigênio dissolvido das espécies). Das 345 espécies de peixes ornamentais para venda, 332 são não-nativos para Minas Gerais (n = 151) ou Brasil (n = 194). Com base nos valores de corte propostos, cinco espécies de peixes ornamentais não-nativos (Cyprinus rubrofuscus, Carassius auratus, Xiphophorus hellerii, Poecilia reticulata e P. latipinna) podem potencialmente invadir os rios Velhas e Muriaé, quatro espécies (C. rubrofuscus, C. auratus, X. helleri, P. reticulata) podem invadir o rio Uberabinha, quatro espécies selecionadas (Cyprinus rubrofuscus, Carassius auratus, X. maculatus e P. reticulata) podem invadir o rio Sapucaí-Mirim, três espécies (Carassius auratus, X. hellerii e P. reticulata) podem invadir o rio Doce, e três espécies (Cyprinus rubrofuscus, P. reticulata e Amatitlania nigrofasciata) podem potencialmente invadir o rio Todos os Santos. Seis recomendações são sugeridas para reduzir o risco de invasão por peixes não-nativos nos rios pesquisados, representado pelo comércio de peixes ornamentais. Key words: Aquarium shops, Aquarium dumping, Fishkeeping, Invasion risk assessment, Non-native fishes. 1Universidade Federal de Minas Gerais, Programa de Pós-Graduação em Ecologia, Conservação e Manejo de Vida Silvestre, Av. Antônio Carlos, Pampulha, 6627, 31270-901 Belo Horizonte, MG, Brazil. [email protected] 2Universidade Federal de Minas Gerais, Departamento de Biologia Geral, Instituto de Ciências Biológicas, Av. Antônio Carlos, Pampulha, 6627, 31270-901 Belo Horizonte, MG, Brazil. [email protected] 433 434 Invasion risks posed by ornamental freshwater fish trade Introduction Material and Methods Worldwide, keeping freshwater and marine ornamental fish Predicting potential invaders in six rivers of Minas Gerais in aquaria is a popular hobby in both homes and public spaces. State. A model was applied to predict probable non-native fish Currently, the global ornamental fish trade generates about invasions through aquarium fish trade in rivers of Minas Gerais US$ 3 billion/year and an equipment and literature industry State. This southeastern Brazilian state is the fourth in size, that exceeds US$ 15 billion/year (Dawes, 2001). In spite of the and the second most populous, with a current population of popularity of fishkeeping, not all amateurs persevere in more than 18 million (Alves et al., 2007). A donor source of adequately caring for their aquaria due to unwelcome species, represented by ornamental fish trade, was identified difficulties such as excessive growth of individuals and and adopted as a vector for deliberate human dumping, in order aggressiveness of some species. Upon giving up their hobby, to create a predictive model that combined biological, historical, many aquarium owners are reluctant to sacrifice their pets, and commercial variables, as proposed by Rixon et al. (2005), and end up discarding them directly in artificial (Fuller et al., with abiotic criteria, as proposed by Chang et al. (2009). 1999) and natural environments (Semmens et al., 2004). The first of these four variables is the invasiveness ability Aquarium dumping, according to Fuller et al. (1999), is of each species, assessed by four parameters: thermal range, the second main cause of non-native species introduction in dissolved oxygen tolerance, type of diet, and parental care or the US. In Brazil, most of the information about fish fecundity (representing reproductive attributes). The introductions concerns escapees from fish farms for food attributes assumed to facilitate the invasion of ornamental production, while reports of aquarium dumping are rare fish were the ability to tolerate changes in water temperature (Magalhães, 2010). Attention has been paid to non-native and dissolved oxygen levels, omnivorous diet (feeding on at ornamental fish species in Brazil, as well as elsewhere in the least two items among organic debris, micro- or macrophytes, world, only after they have settled into a new environment micro- or macro-invertebrates) and either parental care (by (Alves et al., 2007). Once established, it becomes virtually male, female, or both) or high fecundity (high numbers of impossible to eradicate aquatic species (Gozlan et al., 2010). oocytes). These are important prerequisites for the In order to prevent future invasions in Brazilian water bodies establishment of ornamental non-native species in any via aquarium trade, it is necessary to identify species of freshwater body (Moyle & Marchetti, 2006). The second ornamental fish that pose high invasion risks, as well as to variable is the history of worldwide invasions, adapted from monitor the events that may lead to these introductions (such Drake (2007), defined as H = Pe/Pi ×100, where H = history of as new species offered by the market, environmental changes, invasions, Pe = number of countries where the species has and urban growth). successfully established itself, Pi = number of countries where According to Bomford & Glover (2004), simple risk the species was introduced. The third variable is propagule assessment models that predict invasion risk by non-native pressure, estimated by the number of individuals released, a species are a low-cost alternative to guide management primary factor in establishment success (Vander Zanden & policies. Risk models were originally developed to deal with Olden, 2008). Assuming that popular species (i.e. hardy and chemical pollution, and have only recently been adapted for easy to feed) sold in considerable numbers (> 100 specimens other stressors, including non-native species (Calado & per month) have a greater probability of being released in the Chapman, 2006). Invasion risk models by non-native environment by hobbyists, we used the annual frequency of ornamental fish exist for temperate regions, such as those of occurrence in stores, and number